Evolutionary origin of vertebrate OCT4/POU5 functions in supporting pluripotency

Woranop Sukparangsi, Elena Morganti, Molly Lowndes, Hélène Mayeur, Melanie Weisser, Fella Hammachi, Hanna Peradziryi, Fabian Roske, Jurriaan Hölzenspies, Alessandra Livigni, Benoit Gilbert Godard, Fumiaki Sugahara, Shigeru Kuratani, Guillermo Montoya, Stephen R. Frankenberg, Sylvie Mazan () and Joshua M. Brickman ()
Additional contact information
Woranop Sukparangsi: University of Copenhagen
Elena Morganti: University of Copenhagen
Molly Lowndes: University of Copenhagen
Hélène Mayeur: CNRS, Sorbonne Université, Biologie Intégrative des Organismes Marins, UMR7232
Melanie Weisser: University of Copenhagen
Fella Hammachi: University of Edinburgh
Hanna Peradziryi: University of Copenhagen
Fabian Roske: University of Copenhagen
Jurriaan Hölzenspies: University of Copenhagen
Alessandra Livigni: University of Edinburgh
Benoit Gilbert Godard: CNRS, Sorbonne Université, UPMC Univ Paris 06, FR2424, Development and Evolution of Vertebrates Group, Station Biologique
Fumiaki Sugahara: Division of Biology, Hyogo College of Medicine
Shigeru Kuratani: Laboratory for Evolutionary Morphology, RIKEN Center for Biosystems Dynamics Research (BDR)
Guillermo Montoya: University of Copenhagen
Stephen R. Frankenberg: University of Melbourne
Sylvie Mazan: CNRS, Sorbonne Université, Biologie Intégrative des Organismes Marins, UMR7232
Joshua M. Brickman: University of Copenhagen

Nature Communications, 2022, vol. 13, issue 1, 1-21

Abstract: Abstract The support of pluripotent cells over time is an essential feature of development. In eutherian embryos, pluripotency is maintained from naïve states in peri-implantation to primed pluripotency at gastrulation. To understand how these states emerged, we reconstruct the evolutionary trajectory of the Pou5 gene family, which contains the central pluripotency factor OCT4. By coupling evolutionary sequence analysis with functional studies in mouse embryonic stem cells, we find that the ability of POU5 proteins to support pluripotency originated in the gnathostome lineage, prior to the generation of two paralogues, Pou5f1 and Pou5f3 via gene duplication. In osteichthyans, retaining both genes, the paralogues differ in their support of naïve and primed pluripotency. The specialization of these duplicates enables the diversification of function in self-renewal and differentiation. By integrating sequence evolution, cell phenotypes, developmental contexts and structural modelling, we pinpoint OCT4 regions sufficient for naïve pluripotency and describe their adaptation over evolutionary time.

Date: 2022
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DOI: 10.1038/s41467-022-32481-z

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